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PubMed1987

Immunoelectron microscopic localization of photoreceptor-specific markers in the monkey retina.

Antibodies for several molecules that function in the visual process were used to localize these molecules in primate rod and cone cells. These antibodies (monoclonal or polyclonal) were prepared against Interphotoreceptor Retinoid-binding Protein (IRBP), S-antigen (S-Ag), opsin, alpha-transducin and also against cyclic GMP (cGMP). Lowicryl-embedded tissues were labeled with secondary antibodies linked to colloidal gold. Although IRBP is predominantly an extracellular protein, the relatively small amount found intracellularly was localized mainly in rods, with little in cones. Opsin, S-Ag and cGMP were found mainly in rod cell outer segments. A polyclonal antiserum raised against transducin-alpha purified from rod outer segments predominantly labeled rod cells, but an antiserum against the carboxyterminal decapeptide of transducin-alpha labeled both rod and cone cells. Thus, most of these specialized molecules are present predominantly in rod cells, confirming major differences in components of the visual cycle in rods and cones.

Animals↗
PubMed1993

Photoreceptor-specific protein expression of mouse retina in organ culture and retardation of rd degeneration in vitro by a combination of basic fibroblast and nerve growth factors.

Previously we have presented the morphological features of a neonatal mouse retinal explant kept in culture for 3 to 4 weeks. To further evaluate the organotypic parameters of the tissue we have examined the presence of opsin, S-antigen, and interphotoreceptor retinoid-binding protein (IRBP) in the same experimental paradigm, using light microscopic immunocytochemistry. In vitro, opsin and S-antigen staining is found in photoreceptor somata from genetically normal explants and those derived from mice with the rd or the rds mutation. When present, inner and outer segments label more intensely. No IRBP staining has been found in cell bodies of any genotype. However, some labeling is found in the plexiform layers and in the inner segments. The results indicate that photoreceptor proteins are continuously produced in vitro. This further establishes the organotypic nature of the retinal explant in culture. The administration of growth factors to these explants has been investigated. Neither basic fibroblast growth factor nor nerve growth factor alone has affected the explants phenotype. However, the combination of these proteins has significantly retarded rd cell loss in vitro.

Animals↗
PubMed1999

Assessment of Thy-1 mRNA levels as an index of retinal ganglion cell damage.

PURPOSE: Thy-1 is primarily, if not entirely, expressed by the ganglion cells within the retina. This knowledge was used to index ganglion cell death after ischemia and excitotoxicity by studying changes in Thy-1 mRNA levels. METHODS: Insults to the rat retina were delivered either by elevation of intraocular pressure for 60 minutes or by intravitreal injection of N-methyl-D-aspartate (NMDA). After a defined period, changes in Thy-1 immunoreactivity and mRNA levels of Thy-1 and NR1 (NMDA receptor subunit) were used to index ganglion cell sensitivity to damage. Opsin mRNA levels were used as an internal control because photoreceptors lack NMDA receptors. RESULTS: Retinal Thy-1 immunoreactivity, associated with the ganglion cell and inner plexiform layers, is reduced by ischemia or intravitreal injections of NMDA in a dose-dependent manner. Using a semi-quantitative polymerase chain reaction (reverse transcription-polymerase chain reaction) methodology, the levels of total retinal Thy-1 and NR1 mRNAs were shown to be dramatically reduced after both transient ischemia and intravitreal injection of NMDA. The effect of NMDA was found to be both time- and dose-dependent. In contrast, no change occurred in the levels of opsin mRNA unless high levels of NMDA (200 nmoles) were administered. CONCLUSIONS: Ischemia and NMDA-induced excitotoxicity caused retinal ganglion cell destruction, but the photoreceptors were unaffected. Measurement of total retinal Thy-1 mRNA levels provides a useful way of following ganglion cell death especially when combined with immunohistochemical localization of Thy-1. Additionally, the effect on other retinal cell types such as the photoreceptors can be followed in concert using this technique.

Animals↗
PubMed1999

Direct visual resolution of gene copy number in the human photopigment gene array.

PURPOSE: To visualize by direct fluorescent in situ hybridization the entire human visual pigment gene array on single X-chromosome fibers and to compare the results with values obtained by other molecular techniques. METHODS: The size of the opsin gene array on the X-chromosome in eight male subjects was investigated by (i) direct visual in situ hybridization (DIRVISH) on elongated DNA fibers: (ii) quantitation of genomic restriction fragments after Southern blot hybridization; (iii) quantitation of restriction fragment length polymorphism after PCR amplification (PCR/RFLP), and (iv) sizing of NotI fragments by pulsed field gel electrophoresis and Southern blot detection. Each male subject's color vision was assessed by Rayleigh matches on a Nagel Type 1 anomaloscope. RESULTS: The number of genes resolved by the DIRVISH protocol, which ranges from 1 to 6, agrees exactly with the gene array sizes obtained in the same male subjects from pulsed field gel electrophoresis, but differs from the estimates derived from the commonly used indirect Southern blot hybridization and PCR/RFLP quantitation methods. In particular, the PCR/RFLP method overestimates the copy number in all but the smallest arrays. CONCLUSIONS: Visualization of the X-chromosome opsin gene array by DIRVISH provides a new, direct method for obtaining exact copy numbers and helps to resolve the controversy about the range and the average visual pigment gene number in the human population in favor of smaller average array sizes.

Blotting, Southern↗
PubMed2000

Müller cell outgrowth after retinal detachment: association with cone photoreceptors.

PURPOSE: Subretinal gliosis is a relatively common occurrence after retinal reattachment. Because Müller cell processes only intermittently penetrate the outer limiting membrane (OLM) beneath extensive detachments, this study was conducted to determine whether this was preferentially associated with rod or cone photoreceptors. METHODS: Cat retinas were detached from the retinal pigment epithelium and 3 days later were fixed in 4% paraformaldehyde, embedded in 5% agarose, sectioned at 100 microm, and processed for standard immuohistochemistry. The retinas were double labeled with either anti-vimentin and anti-long/medium wavelength-sensitive (anti-L/M) cone opsin or anti-glial fibrillary acidic protein (GFAP) and biotinylated peanut agglutinin (PNA). RESULT: The hypertrophy of Muller cells was readily traced using antibodies to vimentin and GFAP. When labeling with these antibodies was combined with labeling by either antibodies to cone opsins or biotinylated PNA, a consistent relationship was observed between the Müller cell processes growing through the OLM and cone photoreceptors. CONCLUSIONS. The growth of Müller cell processes into the subretinal space forms a fibrotic layer that completely inhibits the regeneration of outer segments. The current results show that there appears to be a highly specific interaction between growing Müller cell processes and cone photoreceptors during the earliest phase in this process.

Animals↗
PubMed2001

A combination of CNTF and BDNF rescues rd photoreceptors but changes rod differentiation in the presence of RPE in retinal explants.

PURPOSE: To gather information regarding the combination of ciliary neurotrophic factor (CNTF) and brain-derived neurotrophic factor (BDNF), compared with the individual factors when used as a treatment to retard photoreceptor cell loss in rd mouse retina explants and to investigate the observation that the retinal pigment epithelium (RPE) influences rod differentiation by this treatment. METHODS: Postnatal day (PN)2 or PN7 control and rd mouse retinas were grown with attached retinal pigment epithelium (RPE). The explants were kept in culture up to PN28. During this culture period CNTF, BDNF, CNTF+BDNF, or vehicle were continuously administered to the culture medium. The nontrophic factors cyclosporin A and N:-CBZ-aspartic acid-glutamic acid-valine-aspartic acid-fluoromethyl ketone (z-DEVD-fmk) were also used. The number of photoreceptor nuclei remaining in the outer nuclear layer (ONL) was analyzed in hematoxylin and eosin-stained sections. Rod- and cone-specific antibodies were used to determine identity and state of differentiation of the photoreceptors. RESULTS: Compared with vehicle treatment, BDNF or CNTF resulted in 1.4- or 2-fold more surviving cell rows in the ONL, respectively. However, when CNTF and BDNF were applied together, surviving ONL cell counts in the rd explants were approximately 3 times those in vehicle-treated explants. In the presence of CNTF or CNTF+BDNF, opsin and arrestin expression in rods was decreased compared with rods without attached RPE. Cyclosporin A and z-DEVD-fmk did not show rescue of rd photoreceptor cells. CONCLUSIONS: CNTF or BDNF treatment of rd retinal explants delays photoreceptor cell loss to some extent. However, when these agents are combined, photoreceptor rescue is much more effective. The quenching of opsin and arrestin expression caused by treatment suggests that simultaneous with rod rescue, rod differentiation is depressed. Regarding retinal degeneration, the results from the selective inhibitors of apoptosis rank the CNTF+BDNF combination treatment as the most consistent and effective experimental pharmacologic intervention currently available.

Animals↗
PubMed2001

An allele-specific hammerhead ribozyme gene therapy for a porcine model of autosomal dominant retinitis pigmentosa.

PURPOSE: To develop a hammerhead ribozyme-based gene therapy for a porcine model of autosomal dominant retinitis pigmentosa (ADRP). METHODS: Hammerhead ribozymes were developed and assayed in vitro against RNA targets homologous to the opsin P347S mutants found in a transgenic porcine model and in humans. Both cloned and synthetic RNA oligonucleotide versions of ribozymes and targets were tested under multiple-turnover conditions using oligonucleotide RNA targets. Digestion of full-length P347S mRNA from porcine retina was performed. RESULTS: The porcine P347S hammerhead ribozyme was specific for the opsin P347S sequence. Multiple-turnover analysis yielded the following kinetic parameters: Vmax=7.3+/-0.5 nM/min, Km=2.1+/-0.6 mM, and kcat=1.5+/-0.4 min-1. The human P347S hammerhead ribozyme was substantially less active (~10,000 fold). CONCLUSIONS: We have developed a hammerhead ribozyme to use as a model for gene therapy of autosomal dominant retinitis pigmentosa in a transgenic porcine model. Based on kinetic characterization of this ribozyme compared to others used for gene therapy, this should be an effective reagent RNA. The allele specific ribozyme we tested for the human sequence, however, is not likely to be useful for gene therapy indicating that an alternative approach is necessary.

Alleles↗
PubMed2001

Action spectrum for melatonin regulation in humans: evidence for a novel circadian photoreceptor.

The photopigment in the human eye that transduces light for circadian and neuroendocrine regulation, is unknown. The aim of this study was to establish an action spectrum for light-induced melatonin suppression that could help elucidate the ocular photoreceptor system for regulating the human pineal gland. Subjects (37 females, 35 males, mean age of 24.5 +/- 0.3 years) were healthy and had normal color vision. Full-field, monochromatic light exposures took place between 2:00 and 3:30 A.M. while subjects' pupils were dilated. Blood samples collected before and after light exposures were quantified for melatonin. Each subject was tested with at least seven different irradiances of one wavelength with a minimum of 1 week between each nighttime exposure. Nighttime melatonin suppression tests (n = 627) were completed with wavelengths from 420 to 600 nm. The data were fit to eight univariant, sigmoidal fluence-response curves (R(2) = 0.81-0.95). The action spectrum constructed from these data fit an opsin template (R(2) = 0.91), which identifies 446-477 nm as the most potent wavelength region providing circadian input for regulating melatonin secretion. The results suggest that, in humans, a single photopigment may be primarily responsible for melatonin suppression, and its peak absorbance appears to be distinct from that of rod and cone cell photopigments for vision. The data also suggest that this new photopigment is retinaldehyde based. These findings suggest that there is a novel opsin photopigment in the human eye that mediates circadian photoreception.

Adolescent↗
PubMed2002

Mouse cone arrestin expression pattern: light induced translocation in cone photoreceptors.

PURPOSE: Arrestins are a superfamily of regulatory proteins that down-regulate activated and phosphorylated G-protein coupled receptors (GPCRs). Cone arrestin (CAR) is expressed in cone photoreceptors and pinealocytes and may contribute to the shutoff mechanisms associtated with high acuity color vision. To initiate a study of CAR's function in cone phototransduction, the mouse CAR (mCAR) transcript and protein expression patterns are examined and in vitro binding assays are also presented. METHODS: Tissue distribution of mCAR was determined by Northern and immunoblot analyses and its cellular localization identified by In situ hybridization and immunohistochemistry. The protein expression pattern of mCAR in the postnatal developmental and adult mouse retina was analyzed by immunoblotting in normal C57 and rd/rd mouse retinas. In vitro binding assays with in vitro translated arrestins were used to study the interaction of mCAR and mouse S-antigen (mSAG) with embryonic chicken outer segment (OS) membranes containing both rod and cone opsins. RESULTS: MCAR has a high level of amino acid sequence identity with orthologous sequences reported for other species except the C-terminal region, which is highly conserved between mouse and rat but divergent in other species. MCAR is expressed exclusively in the retina and the pineal gland, and unique isoforms are expressed during postnatal development of the retina and the pineal gland. The postnatal developmental expression pattern of mCAR and mSAG in the rd/rd mouse retina parallels the generation and degeneration of the cone and rod photoreceptors in these mice. In situ and immunohistochemistry both reveal cone-specific expression of mCAR in the retina. Immunofluorescent staining of retinal sections from dark-adapted or light-exposed mice suggests a light-dependent translocation of mCAR immunoreactivity from the cone inner segments (CIS) and other parts of the cell body to the cone outer segments (COS), similar to but not as dramatic as rod arrestin. In vitro binding assays show a small yet significant increase in binding of the full-length mCAR (mCARFL) to embryonic chicken OS membranes following light activation and phosphorylation of the opsins in the membranes. CONCLUSIONS: MCAR is expressed in retinal cone photoreceptors and the pineal gland. The light-dependent translocation of mCAR immunoreactivity and the increase of mCAR binding to light-activated, phosphorylated embryonic chicken OS membranes, compared to its binding to dark, unphosphorylated membranes, suggest the possibility that mCAR is involved in shutting off the phototransduction cascade in cone photoreceptors as rod arrestin does in rod photoreceptors. However, prominent differences exist between rod arrestin and CAR, suggesting other functions for CAR.

Animals↗
PubMed2003

Non-rod, non-cone photoreception in rodents and teleost fish.

Until recently, all ocular photoreception was attributed to the rods and cones of the retina. However, studies on mice lacking rod and cone photoreceptors (rd/rd cl), has shown that these mice can still use their eyes to detect light to regulate their circadian rhythms, suppress pineal melatonin, modify locomotor activity and modulate pupil size. In addition, action spectra for some of these responses have characterized a novel opsin/vitamin A-based photopigment with a lambda(max) approximately 480 nm. Electrophysiological studies have shown that a subset of retinal ganglion cells are intrinsically photosensitive, and melanopsin has been proposed as the photopigment mediating these responses to light. In contrast to mammals, an inner retinal photopigment gene has been identified in teleost fish. Vertebrate ancient (VA) opsin forms a photopigment with a lambda(max) between 460-500 nm, and is expressed in a sub-set of retinal horizontal cells, and cells in the amacrine and ganglion cell layers. Electrophysiological analysis suggests that VA opsin horizontal cells are intrinsically photosensitive and encode irradiance information. In contrast to mammals, however, the function of these novel ocular photoreceptors remains unknown. We compare non-rod, non-cone ocular photoreceptors in mammals and fish, and examine the criteria used to place candidate photopigment molecules into a functional context.

Amino Acid Sequence↗
PubMed1990

Orientation of retinal in bovine rhodopsin determined by cross-linking using a photoactivatable analog of 11-cis-retinal.

A photoactivatable analog of 11-cis-retinal has been used to probe the orientation of retinal in bovine rhodopsin. The analog binds to the opsin to regenerate a chromophore with lambda max at 458 nm. The linkage site of the analog to the opsin was confirmed to be Lys-296 as in 11-cis-retinal rhodopsin. The analog-reconstituted rhodopsin activated transducin and was phosphorylated by rhodopsin kinase on illumination. On photolysis of rhodopsin containing the radioactively labeled analog at 365 nm at -15 degrees C, 20-25% of the analog was covalently linked to the protein. Proteolysis of the labeled protein and characterization of the appropriate peptides showed that cross-linking of the analog was predominantly to helices C or F. When analog reconstituted rhodopsin in rod outer segments was photolyzed, cross-linking was predominantly to helix C. However, when analog-reconstituted rhodopsin, purified in lauryl maltoside, was photolyzed, labeling occurred mainly in helix F. Sequence analysis showed major sites of cross-linking to be Phe-115, Ala-117, Glu-122, Trp-126, and Ser-127 in helix C while Trp-265 was the major site in helix F. The results suggest that the beta-ionone ring of retinal orients toward helices C and F.

Amino Acid Sequence↗
PubMed1990

Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates.

We have used antibodies specific to either the red/green-or blue-sensitive cones in order to compare their ratio and distributions to that of the rods in the retinae of 3 primate species that differ in their capacity for color vision. We have found that the monoclonal antibody CSA-1 (Johnson and Hageman, 1988) and the polyclonal antibody 4942A, specific to the red- and green-cone opsin (Lerea et al., 1989), applied to retinal whole-mounts labeled approximately 90% of all cones in the diurnal Old-World rhesus monkey (Macaca mulatta) and all of the cones in the nocturnal New-World owl monkey (Aotus trivirgatus) and nocturnal prosimian bushbaby (Galago garnetti). The polyclonal antibody 108B, specific to the blue-cone opsin (Lerea et al., 1989), labeled about 10% of the cones across the entire surface of the rhesus monkey retina, but failed to label any cones in the retina of the 2 nocturnal species. Only the retina of the rhesus monkey possessed an all-cone foveola in which the density of cone inner segments was 17-fold greater than that in the fovea of the owl monkey or bushbaby retina. Surprisingly, the density of cones per unit area outside of the fovea was comparable in all 3 species. Rod density in the dorsal retina was elevated in all animals examined, but was 2-3 times greater in the nocturnal species than in the rhesus monkey retina. Application of the photoreceptor-class-specific antibodies may provide further insights into the evolution and development of wavelength sensitivity in the retina, as well as enhance our understanding of normal and abnormal color vision in humans.

Animals↗
PubMed1989

Transplantation of photoreceptors to light-damaged retina.

We investigated the possibility of reconstructing light-damaged retinas by photoreceptor transplantation. The outer nuclear layer containing the photoreceptor cells was eliminated in adult albino rat retinas by exposure to constant high-level illumination. Photoreceptors for transplantation were harvested from neonatal rats using a novel isolation technique that maintained the cellular organization of the outer nuclear layer. Transplantation was accomplished using a transcorneal approach to the subretinal space, which minimized trauma to the eye. The retina reattached to the back of the eye with transplanted photoreceptors interposed between the retina and the overlying tissues. Prelabelling with fluorescent dye enabled positive identification of the transplanted cells. The transplanted photoreceptors appeared to survive transplantation for at least 6 weeks and were immunohistochemically reactive for opsin. The antibody staining for opsin identifies the transplanted cells as photoreceptors and indicates that they are still capable of producing visual pigment and therefore may have the capacity to transduce light. These findings indicate that photoreceptors can be transplanted to form a new outer nuclear layer in a damaged mature retina.

Animals↗
PubMed1989

Postnatal development of photoreceptor proteins in mutant mice and Abyssinian cats with retinal degeneration.

Using immunocytochemical techniques, development of opsin, transducin alpha and S-antigen in photoreceptor cells of the mice homozygous or heterozygous for the rd or rds genes has been found to be similar to that of control animals during the first postnatal week. Even though the absolute amounts of these proteins are low (eg. opsin in the rds retina) or decrease in the postnatal period (as in the rd retina), we can demonstrate their persistence during the entire degeneration process. In fact, the content of the proteins in the photoreceptor perikarya actually appear to be higher after postnatal day 11 in all mutants studied. Thus, one of the major manifestations of the mutant retinae is a loss of polarity of the photoreceptor cells at the time of ROS degeneration without a loss in the ability to synthesize these important proteins of the visual cycle. This correlates well with the apparent defect in IRBP secretion and its intracellular accumulation in mutant photoreceptor cells as previously observed (van Veen et al. 1986). In the Abyssinian cat model for progressive retinal atrophy, the development an cellular distribution of all the proteins studied are similar in affected and control retinae until the beginning of stage 2 of the disease. At this time, outer segments begin to degenerate and immunoreactivity increases in the photoreceptor perikarya. The IRBP content of the retina declines markedly at stage 2, preceding extensive loss of photoreceptors.

Aging↗
PubMed1988

Identification of proteins in retinas and IPM from eyes with retinitis pigmentosa.

Opsin, the alpha-subunit of transducin, S-antigen, interphotoreceptor retinoid-binding protein (IRBP) and cathepsin D were assessed in autopsy eyes from patients with retinitis pigmentosa (RP) and normal autopsy eyes. Immunochemical methods were used to determine the presence of these proteins on Western blots of retinal homogenates from five RP donors and on blots of interphotoreceptor matrix (IPM) preparations from six other RP eyes. The amounts of immunoreactive opsin, S-antigen, alpha-transducin, and IRBP appeared below normal in retinas from RP eyes. All six IPM samples from patients with advanced RP had reduced amounts of S-antigen and no detectable IRBP or transducin. Cathepsin D (an RPE protein) was present in IPM or RP eyes in amounts comparable to that in IPMs from normal eyes. Small amounts of cathepsin D were also detected in retinas from both normal and RP eyes. These studies show that proteins specific to the photoreceptor-pigment epithelium complex in normal eyes can be detected in autopsy eyes from patients with RP and suggest that the observed reductions in photoreceptor-specific proteins occur as a consequence of photoreceptor loss.

Adult↗
PubMed1982

Pathogenesis of progressive rod-cone degeneration in miniature poodles.

Visual cell pathologic changes and outer segment renewal were investigated in miniature poodles with progressive rod-cone degeneration. Early in this disease, visual cells in the posterior pole and equatorial regions show outer segment lamellar disorientation and vesicular profiles. Visual cells are normal in the periphery. Outer segment renewal determined after intravitreal injection of 3H-leucine was abnormally slower in affected animals than in controls. This renewal abnormality was similar in structurally normal and diseased photoreceptors, suggesting that the renewal defect is the earliest recognizable abnormality in the disease. The pigment epithelium was normal; the presence and density of pigment did not appear to affect the extent and severity of the disease or modify the abnormal renewal rate. As the disease progressed, photoreceptor outer segments were lost, and the remaining diminutive photoreceptors accumulated label in the inner segment and perinuclear zones. Sodium dodecyl sulfate gel electrophoresis of crude rod outer segment preparations showed no differences in opsin synthesis between normal and affected retinas early in the disease, but opsin synthesis decreased in the late stage of the disease.

Animals↗
PubMed1982

Membrane addition to rod photoreceptor outer segments: light stimulates membrane assembly in the absence of increased membrane biosynthesis.

The effect of light on the biosynthesis and the assembly of rod photoreceptor outer segment membranes was analyzed in vitro using retinas from Xenopus laevis. The number of open discs at the base of the outer segment was used as a morphologic index to evaluate relative differences in rates of membrane assembly. Assembly was stimulated in vitro by light, as evidenced by a greater number of open discs that accumulated in light-exposed retinas than that in retinas maintained under the same conditions but in darkness. Quantitative autoradiography indicated, however, that unlike membrane assembly, the incorporation of 3H-leucine or 3H-mannose into proteins by rods was nearly identical in light-stimulated and dark-maintained retinas. Likewise, the synthesis of opsin, a protein destined for the rod outer segment, was not affected by light. We conclude from these studies that the enhanced rate of outer segment membrane assembly that occurs during the early light phase of the diurnal cycle takes place in the absence of an increase in the rate of biosynthesis of opsin, the major outer segment membrane protein.

Animals↗
PubMed1996

Rhodopsin in immature rod outer segments.

PURPOSE: To test the hypothesis that rhodopsin concentration is low in immature rat rod outer segments (ROS). METHODS: Microspectrophotometry (MSP) was used to assess rhodopsin absorbances in localized regions of isolated ROS from dark-adapted 13-, 19-, and 34-day-old and adult rats. Photopigment was extracted from the retinas of paired eyes in dark-adapted and light-adapted rats. One retina of each pair was treated with 9-cis retinal before extraction of photopigment. Rhodopsin with native 11-cis retinal was extracted from the fellow retina. RESULTS: By MSP, rhodopsin absorbance was low in the short ROS of 13-day-old rats. In 19-day-old rats with ROS lengths approximately equal to those of adults, absorbance was low at the tip, but at the base, it was equal to the high absorbance at both the tip and the base in adults. The 9-cis retinal did not add absorbance to the photopigment extracts of dark-adapted retinas at any age, but it did add absorbance to extracts of the light-adapted retinas at every age. CONCLUSIONS: The MSP results show that the accumulation of rhodopsin in developing rat rods depends on increasing concentrations in localized regions. No evidence of apo-opsin is found in immature rat rods. Thus, in immature ROS regions, the low rhodopsin absorbances suggest that the amount of opsin is also low. Greater disk-to-disk spacing in immature ROS regions than in mature regions could account for these findings.

Aging↗